Download Plant Cytoskeleton: Reinforcing Lines of Division in Plant Cells

Current Biology, Vol. 14, R287–R289, April 6, 2004, ©2004 Elsevier Ltd. All rights reserved. DOI 10.1016/j.cub.2004.03.027
Plant Cytoskeleton: Reinforcing Lines
of Division in Plant Cells
Jaideep Mathur
Cytokinesis in plants has unique features concerned
with defining and maintaining the line of cell division.
Recent studies have identified key cytoskeletal components and events that help to ensure the fidelity of
cytokinesis in higher plants.
The ability to divide is a fundamental property of living
cells. In plants, the presence of a cell wall and absence
of cell migration makes the establishment of the line of
division between daughter cells a critical step, important
for both organ morphogenesis and the overall architecture of the plant body. Somatic cell cytokinesis in higher
plants thus presents certain unique features [1]. Following a stage known as karyokinesis, in which the cell
undergoes nuclear division, a distinct cytoplasmic
domain — the phragmoplast — is defined between the
reforming nuclei. The ring-like phragmoplast effectively
demarcates the ‘division plane’ as it mediates organelle
and vesicular traffic to orchestrate the assembly of a
growing cell-plate that fragments the cell into two.
Intriguingly, in most dividing plant cells the site of
phragmoplast formation, and thereby the future
division plane, is predicted accurately, well in advance
of other cell-division events, by a transiently occurring
‘pre-prophase band’ [1,2]. The pre-prophase band
disappears completely by pro-metaphase, and is thus
temporally well separated from the phragmoplast
assembly that typically occurs during late anaphase.
However, the coincident localization of the preprophase band and the phragmoplast suggest that
the former leaves some sort of imprint in the parent
cell’s memory.
The search for this imprint led to the identification of
another intracellular zone defined between the stages
of pre-prophase band and phragmoplast formation.
This ‘actin-depleted zone’ apparently provides a spatial
reference site for the phragmoplast and may constitute
the ‘memory’ left behind by the pre-prophase band [3].
The pre-prophase band, actin-depletion zone and the
phragmoplast (Figure 1) thus constitute major arrays
that define the division line, and their creation and
maintenance obviously plays an important role in
cytokinesis. But despite excellent descriptions emphasizing their spatio-temporal relationship and interdependence, not much is known about the molecular
factors involved in their creation and maintenance.
Recent studies [4–11] have identified many of the molecular components that play pivotal roles in generating
and/or reinforcing these cytoplasmic landmarks, and
provided fresh insights into the novel cytokinesis
process in plants.
Department of Botany, University of Toronto, 25 Willcocks
Street, Toronto, Ontario, M5S 3B2, Canada.
Dispatch
A number of cytokinesis-defective mutants have
been described in plants ([1,7] and references therein).
The presence of incomplete cell walls in enlarged,
usually multinucleate cells is taken as a characteristic
cytokinesis-linked phenotype (Figure 2). Defects may
result from an inability to form cohesive pre-prophase
bands [8] or to co-align developing phragmoplasts to
the pre-prophase band-designated site [6], or as a
result of aberrant cell-plate assembly [9–13]. These
events may involve molecules as diverse as dynamins
[12], kinesin-like proteins [10], syntaxins [9], Sec1-like
proteins [11] and cell-wall/plate components [7,13].
A study published recently in Current Biology [4] has
added the protein PLEIADE to the list of molecular
players that assemble at the line of division. Mutant
pleiade plants display all the defects typically associated with a cytokinesis defect [8], and enlarged pleiade
cells contain phragmoplasts that are significantly
broader compared to wild-type. PLEIADE localizes initially to the pre-prophase band and then, after chromosome separation, specifically to the cytokinetic
phragmoplast [4]. The cytokinesis defect in pleiade
mutants is attributed to an inability to concentrate the
components required for assembling a cell-plate at the
correct location. PLEIADE is a microtubule-associated
protein, hence its alternative name AtMAP65-3.
Although Müller et al. [4] conclude that PLEIADE
has a specific role in phragmoplast formation, its
localization to the pre-prophase band suggests it also
has an earlier role. This conjecture finds support in a
recent study [14] that dissected microtubule behavior
during pre-prophase band formation in exquisite
detail. Dhonushke and Gadella [14] used the yellow
fluorescent protein (YFP) fused to the cytoplasmic
linker protein CLIP170 to highlight the growing plus
ends of microtubules. By resolving pre-prophase band
formation into distinct stages — initiation, narrowing,
maturation and breakdown — and following microtubule plus-end dynamics, these authors were able to
show that the parameters governing microtubule
dynamic instability change significantly during preprophase band formation.
Dhonukshe and Gadella [14] found that microtubules
in a maturing pre-prophase band are shorter and more
dynamic than usual. The formation of filamentous
cross-bridges between anti-parallel, inter-digitated
microtubules is likely to be a critical factor in narrowing down the pre-prophase band with its complement
of very dynamic microtubules. An inability to form such
cross-bridges might result in a loose, unfocused preprophase band. Other plant members of the MAP65
family to which PLEIADE belongs have been implicated in forming precisely such cross-bridges between
microtubules [15], and the pleiade mutant phenotype
[4,8] emphasizes the necessity of maintaining a tight
line of division. That PLEIADE is not the only MAP
required during cytokinesis is suggested by a similar
localization pattern for MOR1/GEM1, another member
Dispatch
R288
Prophase
A
Cytokinesis
B
Pre-prophase band
C
Actin-depleted zone
Interdigitated microtubules
Actin microfilaments
ADZ
Figure 1. Three spatially linked arrays
that form sequentially to define the line of
site of cytokinesis in a dividing plant cell.
The pre-prophase band (A) and phragmoplast (C) are made up of inter-digitating
microtubules with co-aligned actin microfilaments, whereas the intervening stage
(B) is defined by an equatorial actindepleted zone. In most vacuolated cells
the cell plate may develop in a polarized
manner [20], connecting to one edge of
the cell first before extending to the other
side.
Phragmoplast and
cell plate
Nuclear material
Developing cell plate
Current Biology
of the MAP215 family of proteins [5]. The gem1 mutation affects cytokinesis and cell division pattern at
pollen mitosis.
Abnormally oriented cell plates and aberrant
cytokinesis are also seen in tan1 mutant maize. TAN1 is
a highly basic microtubule-binding protein that displays
domain similarity to the vertebrate APC protein [6]. APC
is known to interact with the microtubule plus endbinding EB1 proteins [16], and three EB1 homologs
have been recently identified in Arabidopsis [17,18].
From the localization of one of these EB1-like proteins,
my colleagues and I [17] suggested that microtubule
plus-ends may interact with endo-membranes and help
in their rapid rearrangement. It would likely be informative to observe the activity of EB1-like proteins during
pre-prophase band and phragmoplast assembly in
pleiade, gem1 and tan1 mutant backgrounds.
An additional feature of the EB1-like proteins is a
calponin homology (CH) domain near the amino
terminus [17]. This CH domain appears somewhat different from those of known actin-interacting proteins,
but it remains possible that the plant proteins also
interact with actin. Indeed certain features of plant
cytokinesis make the identification of a possible actininteracting domain in a protein that localizes to the tip
of a microtubule very interesting. It is known that the
pre-prophase band and phragmoplast are both made
up of co-aligned actin microfilaments and microtubules [2,3]. Actin microfilaments are believed to play
a role in narrowing the pre-prophase band, while the
actin-depletion zone that appears after the breakdown
of the pre-prophase band apparently provides spatial
cues to the later developing phragmoplast [3].
The link between the pre-prophase band, actindepletion zone and phragmoplast has been reaffirmed
by Hoshino et al. [19], who tested the effects of
disrupting actin microfilaments at different stages in a
synchronized tobacco BY2-cell population. When the
actin inhibitor was added before formation of the actindepletion zone, the division plane was significantly
altered. Maintenance of the actin-depletion zone is
obviously vital for defining the precise positioning of the
phragmoplast. Defects in the tan1 mutant have been
attributed to an inability of developing phragmoplasts
to be guided to the former pre-prophase band site.
Moreover, TAN1 localizes to both the pre-prophase
band and the phragmoplast [6], and has a region that
can potentially interact with CH-domain-carrying proteins such as EB1. Though pure conjecture at this
point, the chances that actin-microtubule interactions
during cytokinesis occur via this set of proteins is an
intriguing possibility.
The line of division in plants is already beginning to
look crowded as new molecules are identified.
Considering that variations on the cytokinesis theme,
such as asymmetric and polarized cytokinesis, are
common [20], and that many cytokinesis-defective
mutants do not exhibit global phenotypes, dissecting
the hierarchical relationships between these players is
the obvious challenge for a better understanding of
cytokinesis in higher plants.
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Current Biology
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Figure 2. Cytokinesis defective mutants.
Cytokinesis defects are typically identified by incomplete cell
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